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A Review of Paleozoic and Mesozoic Animal Sounds

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A Review of Paleozoic and Mesozoic Animal Sounds Historical Biology Vol. 20, No. 4, December 2008, 255–287 REVIEW Voices of the past: a review of Paleozoic and Mesozoic animal sounds Phil Senter* Department of Natural Sciences, Fayetteville State University, 1200 Murchison Road, Fayetteville, NC 28301, USA (Received 10 March 2009; final version received 6 May 2009) Here, I present a review and synthesis of fossil and neontological evidence to find major trends in the pre-Cenozoic evolution of animal acoustic behaviour. Anatomical, ecological and phylogenetic data support the following scenario. Stridulating insects, including crickets, performed the first terrestrial twilight choruses during the Triassic. The twilight chorus was joined by water boatmen in the Lower Jurassic, anurans in the Upper Jurassic, geckoes and birds in the Lower Cretaceous, and cicadas and crocodilians in the Upper Cretaceous. Parallel evolution of defensive stridulation took place multiple times within Malacostraca, Arachnida and Coleoptera. Parallel evolution of defensive and courtship-related sound production took place in Actinopterygii, possibly as early as the Devonian. Defensive vocalisations by tetrapods probably did not appear until their predators acquired tympanic ears in the Permian. Tympanic ears appeared independently in Diadectomorpha, Seymouriamorpha, Parareptilia, Diapsida and derived Synapsida. Crocodilians and birds acquired vocal organs independently, and there is no anatomical evidence for vocal ability in bird-line archosaurs basal to the avian clade Ornithothoraces. Acoustic displays by non-avian dinosaurs were therefore probably non-vocal. Other aspects of the evolution of acoustic behaviour in these and other lineages are also discussed. Keywords: acoustic behaviour; vocalisation; hearing; Crustacea; Insecta; Orthoptera; Coleoptera; Hemiptera; Crocodylia; Aves; Mammalia Introduction far, most paleobioacoustical research has been concen- The fossil record does not include audio recordings. As a trated on the study of the evolution of hearing in tetrapod result, few researchers lose sleep over such questions as vertebrates (e.g. Reisz 1981; Allin 1986; Wu 1994; Clack whether Triceratops heard crickets chirping in the evening, and Allin 2004; Vater et al. 2004) and the evolution of whether Mesozoic treetops resounded with birdsong or sound production in the insect orders Orthoptera and Hemiptera (e.g. Sweet 1996; Rust et al. 1999; Be´thoux and frogsong, or whether the immense corpses of sauropods Nel 2002; Gorochov and Rasnitsyn 2002). However, many were surrounded by the buzzing of bottle flies. Questions other paleobioacoustical issues can be addressed with such as these seem silly at first but are nevertheless available data from fossil and neontological evidence. For worthwhile to ask for three reasons: (1) inferable acoustic example, the first appearances of fossils of sound- details must be included if the paleontologist is to producing taxa can be used to constrain the times of accomplish one of paleontology’s main goals: the origin of their characteristic sounds. Also, knowledge of reconstruction of the ancient world in as much detail as directional selection on extant animal sounds can be used possible, (2) acoustic signals are of great importance to to infer characteristics of the sounds produced by their Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 many animals, so the reconstruction of the lifestyles of ancestors. In addition, because the functions of animal ancient organisms must take acoustic signals into sounds depend on their reception by the intended consideration, and (3) many studies have addressed recipients, information on the evolution of hearing can whether or not extinct animals could hear (e.g. Reisz be used to constrain the times of origin of certain animal 1981; Wu 1994; Clack and Allin 2004), so it is reasonable sounds. For example, one can reasonably infer that certain to ask what they heard. courtship sounds, territorial sounds and other sounds Bioacoustics, the study of animal sound production directed at conspecifics were absent in taxa that lacked and reception, is a rich field with much to offer the appropriate sensory structures. Similarly, one can also paleontologist for application to the study of sound reasonably infer that certain anti-predator sounds were production and reception in fossil animals. Such absent before the appearance of predators with appropriate application could aptly be called paleobioacoustics. Thus sensory structures. Much information pertinent to the *Email: [email protected] ISSN 0891-2963 print/ISSN 1029-2381 online q 2008 Taylor & Francis DOI: 10.1080/08912960903033327 http://www.informaworld.com 256 P. Senter reconstruction of ancient acoustic behaviour has been published, but before now no attempt has been made to pool available information to illuminate broad trends in such behaviour across large geologic time spans. Here, I present a review of the available literature so as to perform such a synthesis for the Paleozoic and Mesozoic Eras. Major themes in the evolution of aerial sound production and reception Sound reception Most invertebrates are aquatic, and several lineages have independently evolved sense organs that perceive water displacement (Budelmann 1992a,b; Coffin et al. 2004). However, it is difficult to say whether most possess a true sense of hearing, both because the definition of ‘hearing’ varies among researchers and because in aquatic environ- ments the distinctions between sound, vibration and water flow are blurred (Budelmann 1992b). In any case, among extant invertebrates acoustic communication is unknown outside Arthropoda, and there is no reason to believe that the case was different among extinct invertebrates. Airborne sound reception is typically accomplished with tympanic ears. In such ears airborne sounds cause vibrations in a thin membrane, the tympanum (Figure 1), internal to which is an air-filled chamber; mechanoreceptors that are linked to the tympanum detect its movement in response to sounds (Wever 1978; Yager 1999; Kardong 2006). Among insects, tympanic ears have appeared independently in Cicadidae (cicadas), Corixidae (water boatmen), Tachinidae (tachinid flies), Sarcophagidae (flesh flies), Neuroptera (lacewings), Mantodea (mantises), Cicindelidae (tiger beetles), Scarabaeidae (scarab beetles), and several times within Orthoptera (crickets and grasshoppers) and Lepidoptera (moths and butterflies) (Yager 1999; Flook et al. 2000; Robert and Hoy 2000; Cˇ okl et al. 2006) (Figure 2). Tympanic ears in cicadas, water boatmen and crickets are associated with intraspecific acoustic communication Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 (Bailey 1991; Gerhardt and Huber 2002; Cˇ okl et al. 2006). Those of tachinid and flesh flies are used to find their cricket hosts when the latter stridulate (Yager 1999; Robert and Hoy 2000). The tympanic ears of lepidopterans, lacewings, mantises, beetles and grasshoppers are tuned to frequencies Figure 1. Sound production (A–D) and reception (E–H) produced by echolocating bats (Mammalia: Chiroptera), the devices of extant animals. (A) Left cheliped of male ghost crab sounds of which stimulate evasive behaviours in these (Ocypode quadrata), ventral view, showing sound-producing stridulatory structures. (B) Male cicada (Pomponia intermedia) insects (Bailey 1991; Yager 1999; Flook et al. 2000). Such with wings and operculum (exoskeletal covering of tymbal) ears are an evolutionary response to predation by bats removed to show sound-producing tymbal. (C) Sagittally (Bailey 1991; Flook et al. 2000) and, like bats, were sectioned larynx of late-term fetal pig (Sus scrofa) in medial therefore absent before the Cenozoic. Courtship sounds of view, showing sound-producing laryngeal vocal cord and grasshoppers and lepidopterans are secondary and appeared laryngeal cartilages mentioned in text, with edges of airway outlined with broken line. (D) Female katydid (Siliquofera after the advent of tympanic hearing in those taxa (Yager grandis), showing tibial tympanum for reception of airborne 1999), and were therefore absent before the Cenozoic. sound. (E) Head of toad (Bufo americanus), left dorsolateral In addition to receptors attuned to frequencies used in view, showing tympanum for reception of airborne sound. (F) intraspecific communication, some cricket ears also have a Skull of turtle (Trachemys scripta), showing posterior skull Historical Biology 257 Figure 2. Phylogeny of insect orders, after Grimaldi and Engel (2005) showing distribution of sound production and tympanic ears (Dumortier 1963b; Aiken 1985; Yager 1999; Virant-Doberlet and Cˇ okl 2004; Drosopoulos and Claridge 2006). Large symbols indicate wide taxonomic distribution within an order, and small symbols indicate limited taxonomic distribution. Filled circles and squares indicate occurrence within a family or families with known pre-Cenozoic fossil records. A, expulsion of air through spiracles; B, loud flight buzzing; P, percussion of body parts against substrate; S, stridulation; T, tymbals; t, tympanic ears; W, wing fluttering. Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 small number of acoustic receptors for much higher In tetrapod vertebrates with tympanic ears, a bony frequencies produced by echolocating bats (Imaizumi and connection transmits vibrations from the tympanum to the Pollack 1999) (Figure 3), a secondary innovation that inner ear, where resulting fluid vibrations stimulate presumably
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